INTERNAL PARASITES OF THE SEBAGO SALMON 



From BUI<LETIN OF THE BUREAU OF FISHERIES, Volume XXVIII, 1908 



Proceedings of the Fourth International Fishery Congress 



Washington, igo8 




WASHINGTON :::::: GOVERNMENT PRINTING OFFICE 



1910 




Glass .A_ 



SMlM- 



^S: 



INTERNAL PARASITES OF THE SEBAGO SALMON 



From BULLETIN OF THE BUREAU OF FISHERIES, Volume XXVIII, 1908 
Proceedt7!gs of the Fourth lnfernatw?!al Fishej'v Congress : : ]Vashi7!g/o7t, rpo8 




Wo-ruc^l 



WASHINGTON :::::: GOVERNMENT PRINTING OFFICE :::::: 1910 






BUREAU OF FISHERIES DOCUMENT NO. 713 
Issued April. I9I0 



A?R SO W 



a^ 



ej 



INTERNAL PARASITES OF THE SEBAGO SALMON 



By Henry B. Ward, Ph. D. 

Professor of Zoology, University oj Illinois 



Paper presented before the Fourth International Fishery Congress 
held at Washington, U. S. A., September 22 to 26, 1908 



CONTENTS. 

Page. 

Historical survey H53 

Parasites of Atlantic salmon, with tabulated summary 1153 

Parasites of Pacific salmon 1172 

Observations on the Sebago salmon 1173 

Specific relationships- _ 11 73 

Source of parasites 11 74 

A new trematode parasite 11 76 

Cestodes 

Proteocephalus pusillus, nov. sp , 

Sparganum sebago, nov. sp 

Nematodes 

Resum^ and conclusions 

Bibliography 1192 

Explanation of plate ii94 

1152 



INTERNAL PARASITES OF THE SEBAGO SALMON. 

By HENRY B. WARD, Ph. D., 
Professor of Zoology, University of Illinois. 

J» 

In connection with other investigations of the United States Bureau of 
Fisheries in Alaska in 1906, I had the privilege of spending two months in study 
of the parasites of the Pacific salmon. The following year, for comparison of 
the interesting results of this work with similar studies of Atlantic salmon, I 
was designated to join a party engaged in a biological survey of Lake Sebago, 
Maine. During six weeks in this region I examined for parasites a number of 
the Sebago salmon and secured a series of parasites from other fish in the lake 
and adjacent waters. 

The large amount of valuable material obtained on these two trips has 
engaged my entire attention during the interval since it was secured, and even 
yet some questions have not been satisfactorily answered. It forms a most 
interesting contribution to the parasitic fauna of these important fishes and at 
the same time throws some light on the general relations between an animal 
and its parasites, which I hope may be of interest to the scientist and of value 
to the practical fish culturist. This report falls naturally into three parts — 
first, a historical summary, which concerns chiefly the European or Atlantic 
salmon, since this species is the only one that has been studied previous to 
the present date; second, a report on the findings in the case of the Sebago 
salmon, which is very closely related to the European species, together with a 
discussion of the conclusions which may be drawn from these data; and third, 
a similar report on the Pacific salmon, which is less closely related and rather 
widely removed geographically from the other two forms. In the present paper 
are included only the first and second sections of the entire report. 

HISTORICAL SURVEY. 
PARASITES OF ATLANTIC SALMON. 

Rudolphi says that in 1726 Frisch observed a salmon parasite, later known 
as Bothriocephalus solidus, and in 1735 published some record of its occurrence 
in a paper entitled " De taeniis in pisiculo aculeato, qui in Marchia Brandenburgia 
vocatur 'Stecherling.' " This is the first account of a salmon parasite to which 
I have found any reference, and I have been unable to ascertain more precisely 
the data in this case or to verify the reference. 

1 153 



1 154 BULLETIN OF THE BUREAU OF FISHERIiiS. 

The oldest record of a salmon parasite that I have been able to verify is 
found in a paper by Sporing (1753), in which he defends the thesis that inhabit- 
ants of fluviatile regions are more annoyed by tapeworms than those of other 
places, no doubt because of the use of half-raw fish. Of weight for his argument 
is the list of half a dozen fish, including Salmo salar, in which, according to his 
obsers^ations, tapeworm" larvoe are present. The view that man was indebted 
to the salmon for infection with fish tapeworms was generally current in early 
times and, though supported by no scientific evidence, persisted until finally 
thoroughly disproved by Zschokke (1890). Now it may be regarded as fully 
established that man does not acquire a single parasite in any way by the use 
of salmon as food. 

O. F. Miiller (1776, 1777, 1780) was the first to describe and name accord- 
ing to scientific principles some of the parasites from Salmo salar. He named 
Fasciola varica, afterwards called Disioma varicum by Zeder; Echinorhynchus 
salmonis, changed to E. in flatus by Rudolphi; E. Icevis, later changed to E. nodu- 
losus; Tcenia solida, which later became Bothriocephalus solidus Rudolphi, and 
Tcsnia salmonis, later called B. prohoscideus Rudolphi. 

Goeze (1782) gave the first description of Echinorhynchus quadrirostris, 
later more correctly diagnosed and named Tctrarhynchus appendiculatus by 
Rudolphi (1809). Goeze also gave a good description of the encapsulated nema- 
tode lar\'a common in salmon, which he referred to Cucullanus, though doubt- 
fully. Rudolphi afterwards named this form Ascaris capsularia. 

The first formal list of parasites from Salmo salar is that given by Rudolphi 
in 1 8 10, who lists as parasites already recorded for this host eight * species, as 

follows : 

Bothriocephalus prohoscideus. 
Bothriocephalus solidus. 
Tetrarhynchus appendiculatus. 
Distoma varicum. 
Ascaris capsularia. 
Dub. (? Cucullanus). 
Echinorhynchus inflatus. 
Echinorhynchus (?) nodulosus. 

It is of interest to note that Rudolphi records opposite every one of these 
named from six to eight earlier references to the particular species. Five of 
them were originally observed by O. F. Miiller, two by Goeze, and one is a doubt- 
ful species. 

"Braun (1894), who cites the case, says Ligiila larvae, but as this genus has not been recorded for 
Salmo salar I take it to apply only to certain of the host species listed. The original author of course 
did not distinguish even genera in his observations. 

b In the appendix (vol. n, part 2, p. 376) Rudolphi lists another find under the name of Disioma 
crenatum. This material was examined by Liihe (1901, 401) and pronounced not a hemiurid, but fur- 
ther determination could not be made. 



INTERNAL PARASITES OF THE SEBAGO SALMON. II55 

In a later paper (18 19) Rudolphi added to the list no new parasite, Dis- 
toma appendiculatum Rudolphi being merely another name for D. crenatum of 
the appendix in the earlier work. In this list Echinorhynchus fusiformis Zeder 
is only a change of name from E. inflatiis of the earlier list; E. nodulosus is 
omitted; Bothriocephalus solidus is interpreted as introduced by accident when 
its proper hosts chance to be eaten by the salmon. Thus the true list of salmon 
parasites is actually reduced, and numbers only seven in this later list of 
Rudolphi. 

In 1 85 1, Diesing in his "Systema Helminthum" recorded for Sahno salar 

ten parasites, as follows: 

Distomum varicum. 
Stenobothrium appendiculatum. 
Schistocephalus dimorphus. 
Dibothrium proboscideum. 
Echinorhynchus pachysomus. 
■ Echinorhynchus proteus. 
Agamonema capsularia. 
Ascaris capsularia. 
Ascaris clavata. 
Cucullanus elegans. 

Although one notes at once the unfamiliar appearance of the list due to 
numerous changes in the names employed, yet only the last two are actually 
new forms. Thus, in spite of the frequent attention given to the salmon, the 
list of its parasites had only increased from five to ten species in the seventy- 
five years since O. F. Mviller first made scientific records of its parasitic fauna in 
Denmark. 

In 1878 von Linstow in the "Compendium der Helminthologie " listv'd 16 

parasites for Salmo salar. New are : 

Distomum ocreatum Rudolphi. 
Distomum reflexum Creplin. 
Bothriocephalus cordiceps Leidy."* 
Tetrarhynchus grossus Rudolphi. 
Tetrarhynchus solidus Drummond. 

In his "Nachtrag" (1889) the same author includes five new species of 
parasites recorded for Salmo salar since the appearance of the earlier record, 

namely : 

Agamonema communis Diesing. 
Distomum miescheri Zschokke. 
Bothriocephalus sp.? Zschokke. 
Leuckartia sp.? Moniez.' 
Tetrabothrium minimum von Linstow. 

o As indicated in the discussion (p. 1166), this is an error in citation. 

6Moniez (1881) found three cestodes in the pyloric cceca of a salmon obtained in the fish market 
at Lille (France), on which he based a new genus, Leuckartia. Except for the lack of a scolex, the 
specimens agree vieW 'with Bolhrioccplialus injiindibuHjormis, heUer .\bothrium eras sum, to \s\nch they 
may well belong. 



II56 



BULLETIN OF THE BUREAU OF FISHERIES. 



Without tracing in detail the further progress of the record it may 
be said that at the present date the Hst includes 47 species, which are 
enumerated later in this paper. It is of importance for a consideration of the 
distribution of the salmon parasites, the especial object of this paper, to review 
the later studies in this field in their geographic arrangement in order to com- 
pare clearly the parasites found in one area with those which are present in 
another. The salmon which have been most intensively studied are those of 
the Rhine. 

Our knowledge of these forms is due largely to a series of papers by the 
distinguished Swiss helminthologist, Fr. ^schokke, of Basel, which cover the 
work of many years. The first record of Zschokke (1889) included examina- 
tions of 45 fish, of which 42 were found infected with parasites All the fish 
were caught in the Rhine in November, December, and January, and the 
following parasitic species were listed : 



Distomum varicum Zeder 

Distomum reflexum Creplin """ 

Distomum miescheri Zschokke. _II _" ' 

Bothriocephalus infundibuIiformisRudolphi 
Bothriocephalus sp. (larva) . . 
Tetrarhynchus solidus Drummond 
Tetrarhynchus grossus Rudo)phi_ 
Rhynchobothrium paleaceum Rudolphi (iarvaY 
Agamonema capsularia Diesing. _ 

Ascaris clavata Rudolphi '_'_ 

Echinorhynchus sp _ _ _ "_" 



Organ infected. 



CEsophagus _ 



Not a single parasite lay in the alimentary canal below the pyloric coeca 
Monticelh notes that most sharks lose their parasites after a long stay in an 
aquarium, and Zschokke has observed that marine fish otherwise heavily 
mfested lose their intestinal parasites very rapidly when subjected to fasting 
m captivity. The Rhine salmon behaves with regard to parasites just like 
a fasting sea fish. Its parasitic fauna manifests an almost purely marine 
aspect. Fresh-water elements are scanty and insignificant. Clearly, then the 
Rhme salmon takes little or no food during its fresh-water migration. Data 
on individual species close the paper. 

The parasitic fauna of the Atlantic salmon was discussed in extended 
fashion later by Zschokke (i 891) on the basis of his own previous studies and 
those of earlier authors. In all he had examined the viscera of 129 fish caught 
in the Rhine. The alimentary canal contained in all cases the thick yellowish 
or yellow-brown mucus, but never any recognizable remnants of food mate- 
rials, although once plant fibers and undigested remains of a Gammarus pulex 
were found. As m similar previously reported cases, so here also the occur- 
rence of these fragments should be regarded as purely accidental. 



INTERNAL PARASITES OF THE SEBAGO SALMON. 1 1 57 

Only four of the 129 salmon examined were free from parasites, and in 
all 20 species of the latter were recorded from the infested fish. The list of 
parasites recorded is as follows: 

Ascaris adunca Rudolphi. 
Ascaris angulata Rudolphi. 
Ascaris clavata Rudolphi. 
Ascaris (Agamonema) capsularia Diesing. 
Ascaris (.\gamonema) communis Diesing. 
Echinorhynchus acus Rudolphi. 
Echinorhynchus agilis Rudolphi. 
Echinorhynchus proteus Westrumb. 
Distomum varicum Zeder. 
Distomum reflexum Creplin. 
Distomum miescheri Zschokke. 
Schistocephalus dimorphus Creplin. 
Bothriocephalus infundibuHformis Rudolphi. 
Bothriocephalus osmeri (larva) von Linstow. 
Bothriocephalus sp. i (larva)." 
Bothriocephalus sp. 11 (larva). 
Rhynchobothrium paleaceum (larva) Rudolphi. 
Tetrarhynchus solidus Drummond. 
Tetrarhynchus grossus Rudolphi. 

Tetrarhynchus macrobothrius von Siebold ( = Stenobothrium appendicula- 
tum Diesing). 

Five of these species {Ascaris capsularia, Distomum varicum, Bothriocephalus 
infundibuHformis, Rhynchobothrium paleaceum, and Tetrarhynchus macrobo- 
thrius) are abundant, almost regular in their occurrence, while the other forms 
are relatively rare in the Rhine salmon. The common parasites were also 
usually abundant in the individual host; thus 20 to 40 specimens of Ascaris 
capsularia were often found in a single host. Of Distomum varicum, from 30 
to 50 individuals were taken from the oesophagus of one fish. In some cases 
Bothriocephalus infundibuHformis was present in large numbers, but usually 
in one or a few weak, starved specimens. Rhynchobothrium paleaceum and 
Tetrarhynchus macrobothrius occurred in from 20 to 25 individuals in a single 
host. All other parasites were found in small numbers, often only a single 
specimen of any one species. 

Among the 129 Rhine salmon investigated 4 were free from parasites, 55 
sheltered a single species of parasite, and 43 but two species, while 20 had 
three species, 6 had four species, and i had five species of parasites. 

" The various bothriocephalid larvae which occur in the salmon are discussed in a separate paper 
by Zschokke (1890). On the basis of morphologic data he inclined in this paper to the view that five 
dilTerent forms, indicating as many species, might be distinguished. Later studies showed the first to 
belong to Bothriocephalus osmeri von Linstow. This is the form he listed at first (1889) as Bothrio- 
cephalus sp. The second is sp. i of the table, the third and fourth are united as sp. II of the table, 
and the fifth becomes sp. in of the table (see p. 1168). 



1 158 BULLETIN OF THE BIiREAU OF FISHERIES. 

In not a single case was a parasite found in the alimentary canal below 
the pyloric coeca. Indeed, parasites which in other hosts inhabit only the 
intestine, were found in the Rhine salmon to infest stomach and oesophagus, 
as if better protected there than in the vicinity of the anus. The Rhine salmon 
loses its intestinal guests like any fasting fish, and through the exclusion of 
food any new importation of worms is prevented. From the absence of para- 
sites behind the pyloric coeca one may conclude indirectly that Salmo salar 
really fasts in the Rhine. When this species enters the river it is richly laden 
with parasites. It loses its intestinal guests and these are not replaced by 
any new supply. There remain only the natural inhabitants of the anterior 
regions of the canal and those which can withdraw thither. Even these pro- 
tected species diminish in number of species and individuals as the salmon 
remains longer in fresh water and climbs higher in the stream, until finally 
there are left only encapsulated forms. The journey up the Rhine has proved 
at the same time a means of eliminating the intestinal parasites. Some investi- 
gators, although without knowledge of these facts, have yet endeavored to 
explain the migration of many fish as due to the necessity of freeing them- 
selves from parasites acquired in the ocean. 

Salmon caught in Holland, in the lower reaches of the Rhine, are richly 
infested with parasites. Several species were regularly found in large numbers 
and the parasitic fauna recalls strikingly that of the ocean salmon. Distomum 
varicum was very abundant in the oesophagus and Bothriocephalus infundi- 
buliformis in the pyloric coeca. But fish from the upper reaches of the Rhine 
presented a radically different picture. The parasites in oesophagus and 
stomach were very rare. Distomum varicurn had disappeared and Bothrio- 
cephalus itijundibuiijormis appeared only as single, weak, emaciated specimens. 
Often the entire alimentary tract yielded no trace of a parasite. 

The parasitic fauna of the Rhine salmon decreases in proportion as the fish 
ascends the stream. 

A study of the seasonal distribution of parasites in the Rhine salmon 
evidences that the number of species present becomes reduced in the winter 
months, and the number of individuals also falls off markedly. The minimum 
is reached in November and December, the months of spawning, when the fish 
has penetrated farthest upstream. It has lost its unbidden guests on the long 
journey. The maximum of parasitic infection is found in the summer months, 
May to July, when the schools of salmon enter the river. Naturally the journey 
exerts no influence upon those parasites which inhabit closed organs. 

The question next considered is the origin of the salmon's parasites, whether 
marine, limnetic, or indifferent in character. The analysis of the forms recorded 
indicates that the Rhine salmon does not exhibit a single true limnetic parasite, 



INTERNAL PARASITES OF THE SEBAGO SALMON. 



"59 



and its most abundant guests are typically marine. In spite of a long and 
repeated sojourn in the river it does not infect itself with a single fresh- water 
parasite, a fact that indicates strongly the complete fasting of the salmon while 
in the Rhine. In other migratory fish the marine elements become greatly 
reduced or even disappear entirely. Yet tabular comparisons show that in 
contrast with the Rhine salmon all other migratory fish infect themselves in 
fresh water more or less strongly with parasites, thus indicating that whereas 
the salmon fasts in the Rhine, its near relatives feed abundantly on wandering 
from the ocean into the river. 

It was possible to examine also 34 salmon from the Baltic Sea ; all of them 
were infected, and a total of 12 species of parasites were recorded from them, 
as follows: 

Ascaris adunca Rudolphi. 

Ascaris (Agamonema) capsularis Diesing. 

Ascaris (Agamonema) communis Diesing. 

Ascaris aculeati von Linstow. 

Echinorhynchus acus Rudolphi. 

Echinorhynchus pachysomus Creplin. 

Distomum varicum Zeder. 

Distomum appendiculatum Rudolphi. 

Bothriocephalus infundibuliformis Rudolphi. 

Bothriocephalus sp. 11 (larva). 

Bothriocephalus sp. in (larva). 

Trisenophorus nodulosus Rudolphi (larva). 

The Baltic salmon is much more heavily parasitized than the salmon of 
the Rhine. Seven parasites are common to both, and of these five are more 
abundant in the Baltic salmon and two only more abundant in the Rhine 
salmon, while six parasites of the former do not occur in the latter. The rela- 
tive infestation of the two forms is shown in the accompanying synopsis : 



Fish. 


Number 
ined. 


Not 
infected. 


Infested with parasites of given number of species. 




- 


- 


3- 


A- 


s. 




129 
34 


Per cent. 


Per cent. 


Per cent. 
32 5 
23 S 


Per cent. 
16.5 
17.6 


Per cent. 
46 
8.8 


Per cent. 

















Of parasitic species found in the Baltic salmon, Bothriocephalus infundi- 
buliformis was present often in enormous numbers, and the same was true of 
Distomum varicum. On the other hand Ascaris capsularis did not manifest 
the frequence or the abundance already noted for the Rhine salmon. Every- 
thing indicates a rich and uninterrupted consumption of food by the Baltic 



Il6o BULLETIN OF THE BUREAU OF FISHERIES. 

type in contrast with the fasting Rhine fish." Parasites are also found in the 
intestine behind the pylorus, where the Rhine salmon remains free from para- 
sites. Among the intestinal parasites of the Baltic salmon also are included no 
true limnetic species. vSuch only He encapsulated in various organs. This indicates 
that the infection with the true fresh-water parasites, Cucullanus , Tricenophorus, 
Ascaris aculcati, actually occurs in the rivers. The Baltic salmon comes into 
fresh water as richly laden with parasites as the fish caught in the lower stretches 
of the Rhine in Holland. While the parasitic fauna of the Rhine salmon decreases 
in proportion as it ascends the stream, that of the salmon in many other rivers 
is enriched by numerous limnetic elements. The natural explanation lies in 
the fasting of the Rhine salmon, whereas its relatives in other streams do not 
cease taking food. The Baltic salmon, having returned to the ocean, loses the 
limnetic parasites of the open intestine but retains those located in the closed 
organs of the host. 

The material is too scanty to determine a seasonal distribution, if any 
exists, and in fact the food of the Baltic salmon undergoes little change through- 
out the entire year, so that no general modification would be expected in the 
parasitic fauna, variations being merely of an individual or casual type. 

Upon a careful study of the individual species the parasitic fauna of the 
Baltic salmon manifests a more varied aspect than that of its relative. There 
are 2 pure marine forms, in contrast to 8 in the Rhine salmon, 2 pure limnetic 
species as against not a single one in the other host, 6 parasites found in both 
marine and fresh-water fishes, and 3 parasites found only in the Baltic salmon, 
with a fourth which can not be assigned with certainty to either type of environ- 
ment. It is very striking that the purely marine Tetrarhynchi so abundant in 
the Rhine salmon have not yet been demonstrated in the Baltic fish. These 
relations are indicated in the appended table of parasites from the European 
salmon, collated from various authors. 

The Rhine salmon shelters a purely marine parasitic fauna, while the Baltic 
salmon reckons many limnetic forms among its parasitic guests. This remark- 
able condition finds its explanation in the continued feeding of the latter type, 

" One should not forget in estimating this factor as presented by Zschokke that in one important 
respect conditions are not identical. The Baltic salmon are still in salt water; not until they enter 
some estuary and begin the ascent of some river do they meet the fresh water environment to which 
the Rhine salmon investigated by Zschokke are subject. To secure an exact parallel one should 
compare the Baltic salmon with such of the Rhine variety as may be captured in the North Sea. 
Zschokke refers in a later paper to some taken from this body of water and notes in their case also that 
the average degree of infection with parasites is greater than in the case of those fish taken from the 
Rhine stream itself. This fact only emphasizes the immediateness and definiteness of the effect on 
the parasitic fauna of the salmon which is produced by the fresh water environment and abstinence 
from food. 



INTERNAL PARASITES OF THE SEBAGO SALMON. 1161 

even in fresh water, and the resulting enrichment of its parasitic fauna with 
Umnetic forms when it returns to the sea. 

The parasitic record reflects clearly the manner of life led by any host. 

In all, 2,;^ species have been recorded from this salmon, making the list of 
its parasites one of the longest known for any fish. The list of these is then 
given, as follows: 

Ascaris adunca Rudolphi. 
Ascaris angulata Rudolphi. 
Ascaris clavata Rudolphi. 
Ascaris (Agamonema) capsularis Diesing. 
Ascaris (Agamonema) communis Diesing. 
Ascaris aculeati von Linstow. 
Cucullanus elegans Zeder. 
Echinorhynchus proteus Westrumb. 
Echinorhynchus pachysomus Creplin. 
Echinorhynchus acus Rudolphi. 
Echinorhynchus agilis Rudolphi. 
Distomum varicum Zeder. 
Distomum reflexum Creplin. 
Distomum miescheri Zschokke. 
Distomum appendiculatum Rudolphi. 
Distomum ocreatum Rudolphi. 
Distomum tereticolle Rudolphi. 
Distomum sp. Mcintosh. 
Bothriocephalus infundibuHformis Rudolphi. 
Bothriocephalus cordiceps Leidy. 
Bothriocephalus osmeri (lar\'a) von Linstow. 
Bothriocephalus sp. i (larva) Zschokke. 
Bothriocephalus sp. 11 (lan-a) Zschokke. 
Bothriocephalus sp. in (larva) Zschokke. 
Schistocephalus dimorphus Creplin. 
Triaenophorus nodulosus (lar^^a) Rudolphi. 
Leuckartia sp. Moniez. 
Tetrabothrium minimum von Linstow. 
Rhynchobothrium paleaceum Rudolphi. 
Tetrarhynchus solidus. 
Tetrarhynchus grossus Rudolphi. 

Tetrarhynchus macrobothrius von Siebold ( = Stenobothrium appendicu- 
latum Diesing). 
Tetrarhynchus sp. Mcintosh. 

The paper of Zschokke closes with a detailed discussion of the biology and 
relationships of the individual salmon parasites, including citations of the work 
of previous investigators on these forms. 



Il62 BULLETIN OF THE BUREAU OF FISHERIES. 

In a later paper Zschokke (1896) lists the parasites of salmon caught in the 
Rhine at Basel, including the results of examinations extending over several 
years and embracing 16 species, as follows: 

Bothriocephalus infundibuliformis Diesing. 

Tetrarhynchus solidus Drummond. 

Tetrarhynchus sp. 

Schistocephalus dimorphus. 

Distomum varicum Zeder. 

Distomum appendiculatum Rudolphi. 

Distomum ocreatum Rudolphi. 

Distomum reflexum Creplin. 

Distomum miescheri Zschokke. 

Ascaris clavata Rudolphi. 

Ascaris capsularia Diesing. 

Ascaris sp. 

Ascaris sp. 

Echinorhynchus clavseceps Zeder. 

Echinorhynchus acus Rudolphi. 

Pisicola geometra Linnaeus. 

Unreported previousl}^ are Echinorhynchus clavcvceps Zeder, Pisicola geom- 
etra Linnaeus, and possibly also two undetermined species of Ascaris. Elimi- 
nating forms which do not properly belong to the Rhine at Basel and adding 
species recorded previously, the net result is 1 7 species of parasites in the salmon 
at Basel, or one-third of the total known parasitic fauna of that region. Of 
these 17, 13 are characteristic of the salmon and wanting in other fish there. 
The large majority of the list are of purely marine character and a further 
group is characteristic of migratory fish, leaving nothing of a limnetic type 
save Pisicola geometra, a leech which is merely a temporary ectoparasite. 

This paper records also the results of the examination of additional salmon 
from the North Sea, the lower Rhine, and the middle and upper Rhine, making 
the grand total of 179 Rhine salmon examined by this author. The only new 
parasite recorded is Scolex polymorphus Rudolphi. Again, later, Zschokke 
(1902, p. 128-130) discusses the records of his earlier work without adding any 
new data. 

In studies on the Rhine salmon Hoek (1899) records that he found in the 
young fish an ascarid, according to Fritsch A. clavata, and repeatedly specimens 
of a species of Echinorhynchus which Fritsch names E. pachysomus Creplin, 
though he did not observe it in the young salmon. In Hoek's opinion the forms 
obtained, though not fully grown, agree better with the description of E. proteus 
Westrumb, and indeed with the more limited concept of the name according to 
Hammann. Hoek observed not infrequently that young salmon were infested 
with a leech, Cystobranchus {Pisicola) respirans Troesch, which lived as an 
ectoparasite on the skin. 



INTERNAL PAR.\SITES OF THE SEBAGO SALMON. I163 

Concerning the Baltic salmon, other fragmentary data are also on record. 
Olsson (1867) reported Bothrioccphalus proboscideus Rudolphi as frequent in 
Salmo salar both from fresh and from salt water during April and August. 
Later the same author (Olsson, 1876) listed Distomum appendiculatiim Rudolphi 
as frequent in Salmo salar during August. Again (1893) he reported Distoma 
appendicidatum Rudolphi from the stomach as abundant in July. The material 
came from the Baltic Sea and the Gulf of Bothnia. 

Hausmann (1897) lists from Salmo salar Distomum appendiculatum, D. ocrea- 
tum, D. reflexum, and D. varicum. Among 20 specimens examined 13 only 
were infested with trematodes. 

Miihling (1898) records from Salmo salar in East Prussia six species of para- 
sites, as follows: BothriotcBnia proboscidea, Apoblema appendiculatum, Echino- 
rhynchus acus, Ech. fusiformis, Ech. proteus, and Ech. pachysomus. The first 
two are very common, the others occasional. Ech. jusijormis is cited after 
Neumann. 

G. Schneider (1902) reports the following data concerning salmon parasites 
in Finland: A salmon i m. long, caught November 6, 1900, in the mouth of the 
river, was infested with several hundred individuals of Bothriotania proboscidea 
Batsch, which entirely filled the pylorus portion of the intestine and of the 
pyloric cceca. Otherwise the intestine contained no parasites and no food. A 
second salmon, investigated fresh July 2, 1902, had in the intestine the yoimg 
and adult BothriotcEnia proboscidea Batsch and one Echinorhynchus larva, which, 
however, evidently came from fish that had been eaten. In the stomach of 
this salmon he found Clupca sprattus Linnaeus [p. 18 the name is given as Clupea 
harengus membras L.] and in the intestine remains of digested fishes, probably 
also herring. The synchronus presence of herring remains and of very young 
Botlirioiccnia in the intestine of this salmon confirms fully his formerly expressed 
opinion that the salmon infects itself with tapeworms through eating the 
herring. 

According to Schneider (1902, p. 20), Kessler in a Russian paper leported 
the occurrence of adult Bothrioicpnia proboscidea in the intestine of Salmo salar 
from Lake Onega. This body of water is directly connected with the Baltic 
Sea, where, according to Miihling, as just noted, this species is a very common 
parasite of the salmon. Schneider has also found it abimdant in salmon from 
the Gulf of Finland. 

No doubt some observations have been made on the parasites of salmon in 
the Scandinavian peninsula, but they have thus far eluded my search. 

Concerning the parasites in the British Isles many observations are on 
record. But they concern individual investigations at particular locations, and 
as a rule do not cover any continuous study of the problem. In conseciuence the 
lists are not as complete as those already cited for the Rhine and the Baltic, 



1 1 64 



BULLETIN OF THE BUREAU OF FISHERIES. 



and it is somewhat difficult to draw a precise comparison with the data for the 
latter regions. First may be placed such records as concern streams directly 
connected with the North Sea, and hence with the body of water from which 
the Rhine salmon come. 

Concerning the parasites of salmon in the Tay, Mcintosh (1863) has recorded 
certain data. More than 100 fish were examined, few were entirely free from 
parasites, many were richly infested. The parasitic species were both fre- 
quent and abundant, although only 10 species are definitely recorded, as against 
14 in the Baltic and 20 in the Rhine salmon. The species from Tay salmon 
Mcintosh lists as follows : 

Ascaris (Agamonema) capsularia Diesing. 
Echinorhynchus proteus Westrumb. 
Echinorhynchus pachysomus Creplin. 
Distomum varicum Creplin. 
Distomum tereticolle Rudolphi. 
Distomum sp. 

Bothriocephalus infundibuliformis Rudolphi. 
Tetrabothrium minimum von Linstow. 
Tetrarhynchus macrobothrius von Siebold. 
Tetrarhynchus sp. 

The examination of this list shows clearly that the Scotch salmon combines 
elements from the parasitic fauna of both its relatives, the Rhine salmon and 
the Baltic salmon. The strong and continued infestation of the intestine below 
the pylorus goes to establish the fact that the taking of food is continuous. 

No seasonal distribution of parasites could be noted, but the character of 
the parasitic species was striking. 'One pure marine species and two almost 
equally such, together with five characteristic salmonid parasites, show that the 
major portion of the parasitic fauna is of marine origin. On the other hand, the 
intestinal parasites were in large part not marine, but limnetic forms or such as 
are typical in the salmon. As in the Rhine salmon, so also in the Tay, the marine 
alimentary parasites are gradually lost without being renewed. They are replaced 
by such as are of evident limnetic character. Hence the conclusion of Mcin- 
tosh, based on other evidence also, that the Tay salmon does from time to time 
take nourishment during its stay in fresh water. A comparison of the parasitic 
fauna of the three salmons gives, according to Zschokke, the following: 



Baltic salmon 
Tay salmon.. 



Number of 
parasitic 
species. 



Typical 

for the 

particular 

salmon. 



In other 

migratory 

fish as well 

as the 

salmon. 



I migratory fish als^ 



Both ma- 
rine and 
limnetic. 



INTERNAL PARASITES OF THE SEBAGO SALMON. II 65 

Much later than the work just outlined is a paper by Tosh (1905) in which 
he discusses his work on the internal parasites of the Tweed salmon. The mate- 
rial was collected in 1895 at a single place. The author notes the distinctly 
marine character of the parasitic fauna of this salmon, attributing it to the fact 
that " salmon do not feed in the fresh water of a short river like the Tweed, except 
under extraordinary conditions, when a prolonged stay is imposed upon them." 
In all he lists 1 5 species, as follows : 

Ascaris capsularia Rudolphi. 
Ascaris acuta Miiller. 
Ascaris obtusocaudata Zeder. 
Distoma varicum Rudolphi. 
Distoma oereatum Rudolphi. 
Distoma miescheri Zschokke. 
Echinorhynchus acus Rudolphi. 
Echinorhynchus proteus Westrumb. 
Echinorhynchus angustatus Rudolphi. 
Bothriocephalus infundibuliformis Rudolphi. 
Tetrarhynchus grossus Rudolphi. 
Tetrarhynchus macrobothrius Rudolphi. 
Tetrabothrium minimum (larva). 
Tetrabothrium sp. (larva). 
Tsenia sp. (lar\'a). 

Details are given concerning the frequence, appearance, and biology of 
each form. The most important is held to be Bothriocephalus infundibuliformis, 
which, according to an appended table, occurs in 26.4 per cent of the 892 fish 
examined. It does not seem, in the opinion of Tosh, to be seriously harmful to 
the host and is found in the largest and best-fed fish in numbers ranging from 
I to 6 per host. The tremendous infestations noted by Zschokke apparently do 
not occur in this region in the salmon, although observed in the sea trout. 

The only notices from Ireland concerning salmon parasites are brief and 
also of long standing. Drummond (1838), writing in Belfast, described Tetra- 
rhynchus grossus from the abdominal cavity of the salmon, which he found only 
once, and Tetrarhynchus solidus, new species, from the peritoneum and mesentery, 
which he took from three salmon in July, 1838. 

Somewhat later Bellingham (1844) listed among the entozoa indigenous to 
Ireland the following taken from the salmon, namely: 

Ascaris capsularia, on the peritoneum; also in 14 other species of fish, 
all marine. 

Ascaris clavata, from intestine and peritoneum; also in 9 other species of 
fish, all marine. 

Distoma varicum, from the stomach; common in some localities and seasons, 
rare in others. 

Tetrarhynchus grossus, from the abdominal cavity; entered in this list on 
the authority of Drummond (1838). 



I,l66 BULLETIN OF THE BUREAU OF FISHERIES. 

Tetrarhynchus solidiis, from the abdominal cavity; a single specimen loose 
in peritoneal cavity. 

Bothriocephalus proboscideus, horn intestine and pyloric coeca; exceedingly 
common and most so in largest and fattest salmon. 

One should always recall the relative value of such comparisons as those in 
the preceding pages. The fact that from Irish salmon only 6 species of para- 
sites are recorded, from the Scotch form lo species, from the Baltic form 14 spe- 
cies, and from the Rhine salmon 20 species, is partly accounted for by the amount 
of attention directed to the various forms. Thus the first record concerning the 
Rhine salmon (Zschokke, 1889) listed 11 species of parasites obtained in the 
course of examining 45 specimens of the Rhine salmon. The second record by 
the same author (Zschokke, 1891) included 20 species of parasites from 129 
hosts, and the third record (Zschokke, 1896) gave 23 species of parasites from a 
total of 179 hosts. Of these 136 came from the Rhine itself and 43 from the 
sea. More extended study of any host will increase the list of the parasites 
which it is known to support. 

The same species of fish, Salmo salar, occurs in streams on the western or 
American coast of the Atlantic Ocean. Thus far no one appears to have devoted 
especial attention to the parasitic fauna of the American fish, but some scattered 
references to species found in our American salmon are recorded by different 
authors. No doubt the list can be extended considerably by longer search, 
but so far as I can ascertain the following brief references include all records of 
salmon parasites made on this continent and published up to the present time. 

According to Zschokke (1891) Leidy reported Botlirwcephalus cordiceps 
from the intestine of Trutta salar Linnsus. The reference, which is apparently 
cited from von Linstow (1878), is incorrect both in location and content. Leidy 
(1871) reported on the authority of Professor Hayden "the brook trout, Salmo 
foniinalis, of the headwaters of the Yellowstone River, to be much infested 
with a species of tapeworm * * * from the abdominal cavity, but not from 
the intestinal canal * * *. It belongs to the old genus Bothriocephalus, and 
to that section now named Dibothrium." This new species was named Dibotli- 
rium cordiceps. The species was subsequently studied in detail by Linton. I 
am unable to find any other reference to this parasite in the writings of Leidy 
or any record of its occurrence in any other than the original host, which was in 
reality Salmo mykiss, the Rocky Mountain trout; the adult parasite occurs in 
the intestine of the American white pelican, Pclecanus erythrorhynchus . This 
parasite accordinglv seems to have no relation whatever to the salmon and 
should be eliminated from the list of its parasites. 

In the catalogue of parasites from various collections in the United States 
bv Stiles and Hassall (1894) there are listed from Salmo salar Bothriocephalus 



INTERNAL PARASITES OF THE SEBAGO SALMON. I167 

proboscideus from Berlin in the Stiles collection and Bothriocephalus sp. from 
England in the Hassall collection; no specimens whatever are noted as having 
been taken from autochthonous fish. 

In a list of trematodes from Canadian fishes Stafford (1904) records from 
Salino salar Linnaeus, Derogenes varicus O. F. Miiller, found in mouth, oesoph- 
agus, and stomach; Hemiurus appendiculatus Rudolphi, found in oesophagus and 
stomach; Lecithastcr bothryophorus Olsson { = Apoblema mollissimum Levinsen), 
and Sinistroporus simplex Rudolphi, from the intestine. The fish were appar- 
ently purchased in the markets in Montreal and represent conditions during 
the spring and autumn months of 1903. 

I have found no further references to the parasitic fauna of Salmo salar on 
this continent. The list contains two species not previously recorded for this 
host, and yet it is insignificant in comparison with European records for the 
same host. 

Appended hereto is a tabular list of all parasites hitherto reported from 
Salmo salar, arranged according to the place which the parasites hold in the 
present accepted system. The taxonom}' of these groups is at present in such 
confusion that I have contented myself with entering the names employed by 
the author cited and in making a few inevitable corrections. Any attempt to 
adjust the nomenclature adequately would demand an amount of time beyond 
my present command and an amount of space out of keeping with the rest of 
this article. By the citation in the table of the authority, date, locality, and 
location, the reader is enabled to form at a glance a general opinion regarding 
the importance of any parasite yet reported from the salmon and to follow up 
its record with the minimum delay. 



ii68 



BULLETIN OF THE BUREAU OF FISHERIES. 









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BULLETIN OF THE BUREAU OF FISHERIES. 



PARASITES OF PACIFIC SALMON. 

The list of parasites for Atlantic salmon in America, though small, is much 
more extended than the records concerning the Pacific salmon. While tremen- 
dous numbers of the latter fish, which belong to several species of the genus Onco- 
rhynchus, are taken every year for commercial purposes, apparently no one has 
studied the parasitic fauna or done more than to record casually a few data 
taken during a study of some other factor concerning the species. Kven of such 
notes I have found only a very few. 

In a report on the life history of the Alaska salmon, Bean (1890, and also 
1893) noted a few items concerning parasites. He mentions the presence in 
1889 of numerous intestinal worms in the red salmon and finds that all species of 
salmon [in fresh water?] are more or less covered with parasitic copepoda. 

Much more extensive are the notes made by the brilliant young naturalist 
and student of the Pacific salmon, Cloudsley Rutter, who only a short time 
back met such an untimely death. 

In the course of investigations on the natural history of the quinnat salmon 
in the Sacramento River, Rutter (1902) records some interesting items regarding 
their parasites. A common pest in the adult of this species in fresh water is a 
parasitic copepod which attaches itself to the gill filaments. Usually not 
numerous on a single fish, they yet sometimes destroy the gill filaments almost 
entirely. The intestine of the spawning salmon is frequently inhabited by 
tapeworms extending into the coeca and at times filling them completely. They 
do not occur in the stomach. In 1898 they were much more abundant than in 
1900. Among 200 young salmon examined from fresh- water stations in the 
Sacramento basin in May, 1898, and April, 1899, parasites were found in the 
stomach contents of 31 fish. They were described as of two or three kinds, one 
elongated [cestode?], the others short and grain-like [trematodes?]. Rutter 
thinks that residence in fresh water is conducive to the growth of parasites in 
the stomachs of young salmon. He gives the following tables of their occurrence 
according to size of host and dates of capture. 

Occurrence of Parasites in Quinnat Salmon from S.\cramento River. 
According to dales of caf>ture. 



Month. 


Number 
examined. 


Number with 
parasites. 


Percentage 

with parasites. 




9 

IS 

Is 
■ s 


4 

3 
3 
8 
3 
8 














_ 


May 




July . - 






^ 




J _ 




^ 


November 


20 




" X 






Total- 


209 


31 




■ 





INTERNAL PARASITES OF THE SEBAGO SALMON. 1 1 73 

Occurrence of Parasites in Quinnat Salmon from Sacramento River — Continued. 
According to size of fish. 



Size. 


Number 
examined. 


1 Number w 
parasites 


th 


Percentage 

with parasites. 




61 
57 
53 

30 
8 


3 
3 

1 ^ 




















38 








TotaL 


2og 


1 31 











It will be noted that the percentage of infestation increases rapidly with the 
size and age of the fish, but this would naturally be associated with the more 
extensive feeding of the older and larger fish, whether in fresh or salt water. In 
the absence of comparative data for salt water forms to contrast with these of 
summer residents in fresh water, it is not allowable to attribute this condition 
to the delayed migration of these fish, as Rutter does. From brackish-water 
stations 20 young salmon were examined and parasites found in 3 only. This 
number is too small to be available for comparison with those fresh-water forms 
noted above. Unfortunately no further data are available concerning the 
varieties of parasites found either in the adult or in the young specimens. It is 
probable that the adult parasites are the same as certain forms to be discussed 
later from the Alaska salmon. 

OBSERVATIONS ON THE SEBAGO SALMON. 

SPECIFIC RELATIONSHIPS 

The Sebago salmon is regarded by some as merely a landlocked variety of 
the Atlantic salmon, Salmo salar. found both in European streams and in the 
rivers of Maine and northward. By others it is viewed as a separate species, 
Sahno sebago, but in any event closely related to the former. In their extensive 
catalogue of North American fishes, Jordan and Evermann (1896) include all 
these forms in the single species Salmo salar Linnaeus, speaking of its range as 
follows : 

North Atlantic, ascending all suitable rivers in northern Europe and the regioa 
north of Cape Cod to Hudson Bay; formerly abundant in the Hudson and occasional in 
the Delaware, its northern limit in the Churchill, Albany, and Moose rivers, flowing into 
Hudson Bay; sometimes perfectly landlocked in lakes in Maine and northward, where 
its habits and coloration (but no tangible specific characters) change somewhat, when 
it becomes (in America) vars. sebaqo and ouananiche. Similar landlocked varieties 
occur in Europe. 

Of the Lake Sebago form which I had the opporttmity of studying and 
which these authors regard as a subspecies, Sahno salar sebago (Girard), they 
write as follows : 

Smaller in size, rather more plump in form, and nonmigratory ; not otherwise evi- 
dently different. Sebago Pond and northward; introduced into lakes in various parts 
of the country; seldom entering streams; reaches a weight of 25 pounds. 



1 1 74 BULLETIN OF THE BUREAU OF FISHERIES. 

It is important to notice that the same authors also recognize a second 
subspecies, and this may be the form from which were obtained the parasites 
reported by Stafford (1904) and alread}' commented upon. Concerning this 
subspecies, Jordan and Evermann write that Salmo salar is — 

* ='= ■■■ represented in Lake St. John, Saguenay River, and neighboring waters 
of Quebec by the landlocked Salmo salar ouannmrke McCarthy MS., new subspecies. 
Still smaller, rarely reaching a weight of 7 '2 pounds and averaging 33^. An extremely 
vigorous and active fish, smaller and more active than ordinary salmon, but so far as 
known not structurally different. Saguenay River, Canada (outlet of Lake St. John), 
and neighboring waters. 

Were it possible to determine definitely whether the records of Stafford 
concern the oceanic form caught during its migration or the landlocked form, 
a more definite value could be placed upon his data. In the absence of such 
information one can not venture to use these records at all in the discussion 
of the biological problems concerned. What these problems are will be clearer 
after a more detailed consideration of the case. 

SOURCE OF PAR.'iSlTES. 

In view of the close specific connection of the two forms, the European sal- 
mon just considered and the Sebago salmon, a comparative study of their para- 
sitic fauna is of unusual interest, especially since the Atlantic salmon spends 
the greater part of its life in salt water, and after its entrance into fresh- water 
streams in the course of its migration does not in most cases partake of any food. 
Consequently whatever parasitic guests it harbors must, as already explained, be 
of marine origin. The exceptions to this statement are due to accidental infec- 
tion, and are both small in numbers and insignificant in variety and relative 
importance. On the other hand, the landlocked Sebago salmon never enters 
salt water. Its period of active feeding and growth is passed in inland waters, 
those of Sebago Lake in the case of the specimens we secured and examined. 
Whatever parasites it harbors are hence obtained in that lake, and are either pure 
fresh-water organisms or such as have been introduced with the host and subse- 
quently acclimatized to a fresh-water existence. In the case of such parasitic 
species as undergo direct development, like many nematodes, the introduction of 
a marine parasite into fresh water involves the habituation of the free living stage, 
either egg or larva, or both, to the limnetic environment, and this is the identical 
process involved in the transfer of any free living organism from a marine exist- 
ence to one in fresh water. In the case of parasites which manifest indirect 
development with change of host the case is much more complicated. Such 
parasites usually have one or more brief stages of free existence in the open 
water as egg, embryo, or larva, like those just referred to. But they also employ 
one or more intermediate hosts, in which certain parts of the development are 
passed. Now, either the same marine animals which serve as intermediate 
hosts in the sea must be found in fresh water also, or must be successfully 



INTERNAL PAR.'iSITES OF THE SEBAGO SALMON. 



II75 



introduced at the same time with the primary host and its parasites to which 
they are related, or, finally, there must be present in the fresh water other animals 
which can ser\'e successfully as intermediate hosts. The interrelation is thus very 
complicated and the chance of achieving it so small that in most cases marine 
forms do not bring the majority of their parasites with them in the transfer to 
fresh-water existence. In other words, limnetic animals are less heavily para- 
sitized than marine. For this reason the examination of so recent a migrant 
into fresh water as the Sebago salmon is of great biological interest. 

At Lake Sebago only 7 specimens of the Sebago salmon were obtained and 
examined. These weighed, respectively, 2, 2, 2, 3, 5 J2 , 8, and i6 pounds. While 
the number examined was from one standpoint small, yet in view of the scarcity 
of the species in the lake it was fortunately large. The series was also representa- 
tive of different ages, ranging probably over several years in growth. It seems 
likely that if marked variations in food materials were found such a range of 
specimens would indicate the fact through differences in parasitic infestation. 
Yet there was a striking uniformity in the records in the series. Furthermore, 
the fish were all examined very soon after capture, and thus any post-mortem 
wanderings, which certainly do influence the location of parasites collected 
from market fish, were largely avoided. No doubt there are rare parasites of 
this species which are not represented in this collection, but, all things being con- 
sidered, it may be asserted with some confidence that the records give a true 
picture of the number and location of the parasites infesting them. 

The parasites found are recorded in the following table : 

Record of Parasites from Salmo sebago. 

[x— many. xx=very many. §=niore than in fish no. 14— not counted.) 



Host. 


Parasites, number and location. 


6 
2 


In. 

16 

16 


i 

Lbs. 


& 


CEsopbagus and 
stomach. 


Pyloric coeca and 

adjacent part of 

intestine. 


Intestine behind py- 
loric coeca. 


Body cavity. 


14 


d 


7 Azygia sebago 


45 Abothrium cras- 


I Proteocephalus pusil- 
lus. 

I Azygia sebago 

I Proteocephalus larva. 

I Bothriocephalidlar\'a. 
Proteocephalus pusillus. 
Proteocephalus pusillus _ 

I Bothriocephalid larva- 


I Nematode A. 


15 


13 Azygia sebago 


§ Abothrium cras- 


















16 


27 


8 


d 


XX Azygia sebago a 


70 Abothrium cras- 


I large Bothriocephalid 

larva. 
I small larval cestode 




17 
33 


16 


6 
d 


I Azygia sebago 

18 Azygia sebago 


30+Abothrium eras- 
sum. 
80 Abothrium cras- 








33 Nematode B.& 








19 


2K 

5'A 


d 
d 


XX Azygia sebago 

19 Azygia sebago 


X Abothrium cras- 
50 Abothrium eras- 




encysted in spleen. 
3 Nematode A. 





















ling bladder (?). See text. 



6 Viscera a mass of adhesions; parasites difficult to pick out. 



1176 BULLETIN OF THE BUREAU OF FISHERIES. 

A NEW TREMATODE PARASITE. 

Every one of the 7 fish examined contained specimens of a new trematode, 
which I have named Azygia sebago. It is relativefy insignificant in size and 
difficult to detect amid the thick white nmcus which fines the wall of stomach 
and ojsophagus. Not a single host was without this parasite, and several salmon 
sheltered considerable numbers ; yet in most cases they were not seen in life, but 
only appeared after the stomach and its contents had been agitated in a pre- 
serving fluid. Careful examination of the debris then never failed to disclose 
some specimens of this worm. Moreover, it was the only species of trematode 
that was found in the vSebago salmon. The description of the species may 
properly precede a discussion of its biological characteristics. 

The genus Azygia was established by Looss (1899, p. 569) to include a well- 
known European species, Disiomum tereticolle Rudolphi, which was made the type 
of the new genus. It was also the only species in the genus ; for, as Looss remarks, 
he had not been successful in finding among the flukes that he knew any form 
which could be included naturally with the old species, Distomum tereticolle. 
There are at the disposal of the student several good descriptions and delinea- 
tions of the old species, Azygia tereticoUis Rudolphi, so that it is possible to 
determine with precision its structural features ; the best of these descriptions is 
undoubtedly that by Looss (1894). 

The new species, Azygia sebago, "■ is much smaller than the older form, 
measuring 10 mm. in maximum length and averaging 5 to 6, or less often 8 mm., 
in well-developed specimens. Fortunately, I have a large range of sizes, from 
such as are only barely, over i mm. in length to the maximum noted, so that it 
was possible to follow the changes accompanying the assumption of the adult 
form. Specimens 2.85 mm. long have not yet produced ova. 

The general form of the body is cylindrical, bluntly rounded at the anterior 
end, and tapering slightly toward the posterior end, which, however, is ulti- 
mately rounded oft'. The body is regularly divided into two regions by a shal- 
low furrow at which the direction of the long axis changes more or less (fig. i), 
giving the worm in lateral aspect much the appearance of a can-top tightener. 
While the relation of the regions is very variable, at times forming almost a sin- 
gle straight line and again standing at a considerable angle with each other, yet 
one can make out these conditions even in specimens which are poorly killed and 
badly distorted. The anterior region assumes the form of an ellipse surrounding 
the two suckers. This region changes relatively little in size with growth. In 
one of the smallest specimens measured (1.6 mm.) the distance between the 

"During the spring of 1908 two of my students, Messrs. W. N. Anderson and H. B. Boyden, made 
a study of this form and prepared a partial report on its structure, to which I am indebted for some 
of the data in the following description, and also for two figures. 



INTERNAL PARASITES OF THE SEBAGO SALMON. 1 1 77 

centers of the two suckers was 0.5 mm. In one 10 mm. long this distance 
measured i mm. 

The posterior region is nearly a perfect cylinder until shortly before the 
tip, where it tapers somewhat. In some specimens the posterior end is consid- 
erably inflated and appears semitranslucent. This is undoubtedly due to the 
distended condition of the excretory reservoir, which inhibits contraction of 
the circular muscles in the portion of the skin adjacent to it. 

The breadth of the body varies according to the degree of contraction, but 
may be estimated in general as from 0.7 to i mm. An immature specimen 
2.85 mm. long measured 0.65 mm. in breadth between the suckers, 0.6 mm. 
behind the acetabulum, and 0.52 mm. behind the posterior testis. An imma- 
ture specimen only 1.6 mm. in length measured 0.32, 0.28, and 0.21 mm. in 
breadth at the same points. In cross section the body is round or very 
slightly oval. 

The oral sucker is subterminal and its opening looks almost directly ventrad. 
It is rather conspicuous, and in an average specimen measured 0.68 mm. in 
antero-posterior diameter and 0.67 mm. transversely. The depth in the same 
specimen was 0.6 mm. The orifice is nearly circular, though often appearing 
slightly flattened along the posterior margin. In an immature specimen 2.85 
mm. long the oral sucker measured 0.35 mm. in antero-posterior diameter and 
0.4 mm. laterally ; the orifice measured 80 by i so /i. 

The ventral sucker or acetabulum is usually distinctl}' smaller than the 
oral. In the extreme case it appears about equal in size or, on the other hand, 
only about half as large. Ordinarily it is prominent, but in short, thick specimens 
it is almost hidden, whereas in elongated, slender specimens it projects so far as 
to appear almost pedunculate. It is also often slightly oval in a transverse 
plane. In an adult specimen it measured 0.57 mm. in antero-posterior diameter 
and 0.69 mm. laterally. In a specimen 2.65 mm. long the corresponding meas- 
urements were 0.3 and 0.33 mm., and the orifice measured 52 by 80 /i. 

The alimentary canal opens in the oral sucker, close behind which lies the 
pharynx without any prepharj'nx between the two. The pharynx measures 
0.21 by 0.13 mm. It is often seen in the vertical position represented in the 
figure of Messrs. Anderson and Boyden, which I have taken the liberty of copying 
here. The oesophagus is very short and it often proceeds anteriad from the 
upright pharynx, as shown in the drawing (fig. 3, pi. cxxi). At its tip start the 
two branches of the intestine, which also usually extend forward a short distance 
and then turning posteriad continue almost to the extreme posterior tip of the 
body. These crura being longer than the body in the usual specimen are thrown 
into folds, which often appear as if the canal possessed irregular outpocketings, 
such as one finds in Paragonimus. Observations both on the living material and 



1 1 78 BULLETIN OF THE BUREAU OF FISHERIES. 

on serial sections show positively that such is not the case, but that the crura 
are simple tubes. The number of folds, twists, and turns depends upon the 
degree of contraction and usually appears greatest between the acetabulum and 
the ovary. 

The excretory system is very characteristic of the genus Azygia. An 
elongate carrot-shaped collecting reservoir or bladder extends from the 
excretory pore, which is located at the posterior tip, through the center of the 
body anteriad to the posterior testis. The wall is heavy and is thrown into 
folds which appear at intervals projecting slightly into the cavity. From the 
anterior end of this reservoir two tubes pass off, right and left, which are 
at the start dorsal to the posterior testis; they soon pass toward the ventral 
surface, but cross the acetabulum on its dorsal aspect and dorsal to the oral 
sucker and are reflected posteriad. During their entire course they lie within the 
intestinal crura and usually ventrad to it. Their heavier walls indicate clearly 
that these conspicuous tubes are more nearly analogous to the collecting reser- 
voirs of other flukes than to the delicate excretory vessels which here also are 
seen connecting with the tubes and the reservoir at various points. 

The three germ glands, the ovary and two testes, lie close together in a longi- 
tudinal row distant from the anterior end about two-thirds the length of the 
worm. The ovary is most anterior and smallest of the group. An unusual 
morphological feature is the inclusion of the shell gland, a small yolk reservoir, 
the ends of the yolk ducts, and the first coils of the uterus within the same capsule 
that incloses the gland proper (fig. 6, pi. cxxi). The relation of the ducts as 
worked out by reconstruction is represented in figure 5 after the studies of Messrs. 
Anderson and Boyden. This resembles closely conditions as shown by Looss 
(1894) foi" ^- it^f'cticollis, although I do not find that he has noted the massing of 
organs within a common capsule. The uterus extends forward in numerous short 
coils which all lie within the intestinal crura until at the acetabulum it merges 
into a short, heavy-walled metraterm. The latter passes dorsal to the acetabu- 
lum and ventral to the cirrus pouch into the genital cloaca, with an inconspicu- 
ous genital pore located just anteriad to the acetabulum. 

The vitelline glands lie along either side of the worm exterior to the intestinal 
crura. They begin a little behind the level of the acetabulum and extend to a 
point about halfway from the posterior testis to the end of the body. This 
constitutes perhaps the most striking morphological difference between this 
species and Azygia tereticol/is, in which the vitellaria do not pass posteriad of 
the posterior testis. This conspicuous difference in the extent of the vitellaria 
enables the student to differentiate the two forms at a glance. 

Attention should be called to the fact that on account of this structural 
feature a correction must be made in the generic description of Azygia, in which 



IXTERNAL PARASITES OF THE SEBAGO SALMON. 1 1 79 

stress was originally laid on the extent of the vitellaria. The condition of the 
vitellaria in the older species has also been employed by Pratt (1902) as a char- 
acteristic of the genus in elaborating his key for the determination of the flukes. 
Although typically a member of the genus Azygia, the present form would fall 
in another genus according to the terms of that synopsis. No one who sees a 
specimen or reviews the structure of this form can doubt its relationship; the 
precise extent of the vitellaria is evidently a subordinate feature, and as such 
of specific rank only. 

The follicles of the vitellaria are distinct, regularly oval bodies, lying in 
two longitudinal rows on each side with a more or less conspicuous break oppo- 
site the ovarv between the anterior and posterior series. The follicles measure 
from 0.06 to 0.07 by 0.03 to 0.04 mm. The symmetry of the rows is in places 
interrupted by extra follicles, making at such points three rows of follicles 
instead of two as usual. The ducts from the anterior and posterior series unite 
opposite the ovary to form a common transverse duct which at the center of 
the body joins its fellow from the opposite side. At the point of union there is a 
small yolk reservoir. As already noted, this is included within the common 
capsule which surrounds the ovary and is ordinarily not visible except in sec- 
tions. Laurer's canal is present and opens on the dorsal surface just posterior 
to the ovary. It does not have the enlargement ordinarily called a seminal 
receptacle, but is usually somewhat coiled and lies on the left side of the ovary. 
This may be an adaptation to the extreme variations in length so character- 
istic of this worm. 

The eggs are small; an average of 50 measurements places their size at 48 
by 27 iJL, which is slightly larger and broader than those of .4. tereticollis, accord- 
ing to the measurements given by Looss (1894). 

The testes are oval bodies lying one directly behind the other and that 
behind the ovary. The three organs are separated only very slightly from each 
other. The outline of the testes is smooth and measures 0.42 to 0.46 by 0.59 
to 0.6 mm. with the major axis transverse. One can usually distinguish that 
the two are not equal in size. The coiled seminal vesicle and a poorly devel- 
oped cirrus with prostate lie in a common connective tissue capsule, the cirrus 
pouch, which stands immediately anterior to the acetabulum. The pouch 
measures about 0.23 by 0.17 mm. in diameter. It opens anterior to the metra- 
term into the genital sinus already mentioned. 

One histological feature deserves consideration here because of its con- 
spicuous character. In sections of Azygia sebago one notices certain muscle 
elements which are so prominent and regular as to deserve almost the name of 
a layer; they occur within the parenchyma, far removed from the usually rec- 
ognized dermal layers and at a point where ordinarily one finds only scattered 



Il8o BULLETIN OF THE BUREAU OF FISHERIES. 

dorso - ventral or oblique fibers which are not subject to any regularity in 
arrangement. These are longitudinal fibers extending from the oral sucker 
throughout the entire length of the distome, as is clearly seen in a frontal section 
(fig. 4, pi. cxxi). In position they lie one-fourth to one-fifth the radius of the 
section distant from the external surface. The cross sections of these fibers 
show them to be much heavier than the other muscle elements and to occupy 
an oval zone parallel to the outer surface of the body. They divide the body 
accordingly into a cortical and a medullary portion. The vitellaria are the only 
conspicuous organs which lie in the cortical layer. This muscle layer is 
undoubtedly related to the marked contractions of the fluke which have already 
been commented upon. Unfortunately I have no material available from 
which to determine whether similar fibers also exist in .4. tereticoUis. Looss 
(1904) does not mention them. 

The relations of oral sucker, pharynx, and crura, the convolutions of the 
intestinal branches, the coils of Laurer's canal and of various ducts and the 
sinuous course of the collecting tubes in the excretory system all point toward 
the variable extensibility of the worm. Differences in caliber and in the dis- 
tance between organs also indicate the same. Observations on the living 
parasite serve to show that it is constantly extending and contracting the body 
to such an extent as to double or halve the length within a few seconds of time. 
In fact, I have never before observed a form which indulged in such energetic 
twisting and contracting. This habit renders any observations on the living 
worm very difficult. 

Looss (1894, P- 7) comments on the active migration of .4. tereticoUis after 
the death of the host, a feature previously recorded for D. cylindraceum by 
Braun (1890, p. 568). .4. sebago manifests the same tendency in the most 
marked degree. The normal seat of this parasite I feel sure is the stomach, 
and perhaps the oesophagus also, but even a slight delay in the examination of 
the host resulted in finding single specimens well down the intestine as well as 
up in the pharynx and even among the gill filaments. In one case a salmon 
caught late in the day was kept overnight to be photographed, as it was a 
peculiarly fine specimen. When the viscera were examined, about twenty 
hours after the capture of the fish, my field notes record that there were 36 dis- 
tomes in the air bladder and that they were seen coming in through the ostium 
with mucus from the oesophagus. Other specimens were found in the pharynx 
and gill cavity and one even in the body cavity. The last can be attributed 
no doubt to some tear in the alimentary lining which permitted the fluke to 
make its way unhindered into what is ordinarily a closed cavity. In still 
another salmon which had gorged itself on smelts my field notes contain com- 



INTERNAL PARASITES OF THE SEBAGO SALMON. I181 

ments on the activity manifested by these distomes, which cHmbed about on 
the smelts and in them as they lay half digested in the stomach of the 
salmon. 

This was so noticeable that I turned my attention at once to the smelt " to 
ascertain if perchance it played any part in the life history of the distome. In 
all, I have records of 52 smelts examined, and in 46 of these were found speci- 
mens of Azygia sebago. The parasite occurred in the stomach only and the 
infestation was small, from i to 14 distomes being found in each host, with an 
average of only 4 to a fish. In most cases the parasites which were taken from 
the stomach of the smelt were immature, not having yet reached that size at 
which the production of ova begins; they were on the average 3 to 4 mm. long, 
or in some cases even smaller, running from 1.5 to 2.5 mm. in length. Single 
specimens reached a length of 6, 7, and even 10 mm. In one case, indeed, there 
were none shorter than 6 mm., and the specimens varied from that to 10 mm., 
so that one can not fairly maintain that they never reach the size attained in 
the salmon. Nevertheless, after the account is cast up the average shows dis- 
tinctly that the distomes do not reach their full size in the smelt and, so far as 
collections made during July and August can indicate, those taken from this 
host are usually small in size and sexually immature. I did not obtain any 
information as to the source from which the smelt acquires its infection, but in 
view of the universality with which smelt form the food of the salmon in Sebago 
Lake the latter undoubtedly owe to them the major portion of their infestation 
with this parasite. 

The host record of Azygia sebago is even yet unfinished. In the course of 
my work numerous other fish from these same waters were examined. In 
young specimens of Esox reticulatus 6 to 16 inches long I found this same para- 
site reasonably abundant. To be sure, they seemed to average somewhat longer, 
being 10 to 12 mm. in length in material from one host and 10 to 14 or even 18 

oThis fish I am compelled to designate under the name Osmerus mordax (Mitchill), as Jordan and 
Evermann (1896) do not recognize the Sebago smelt as a separate form, saying of the species "Atlantic 
coast of the United States from Virginia northward to Gulf of St. Lawrence, entering streams and 
often landlocked." I am inclined to think that even in Sebago Lake there are two smelts. My atten- 
tion was first directed to this possibility by Dr. W. C. Kendall, who, recalling our previous discussion, 
writes as follows in a recent letter: 

"You may recall that there seem to be two forms in the lake differing somewhat in size and habits. 
The large form, which is the one that we caught with hook and line, is nearer to the marine smelt. 
The small form is the one that we found in the salmons' stomachs. You will doubtless recall that the 
principal food, when any at all was found in their stomachs, of the large form was small fish, generally 
young smelts. Our examinations of the stomach contents of the small form show Entomostraca almost 
exclusively. This difference is indicated also by the gillrakers, which are more numerous in the small 
form." 

These distomes occurred equally in both sorts of smelt and those from the smaller smelts were 
larger than those from the larger fish. This is, of course, a mere accident, but it serves to show that 
the two types of smelt conduct themselves alike toward the parasite. 



Il82 BULLETIN OF THE BUREAU OF FISHERIES. 

mm. long in that from another host. In the latter it was noticeable that the 
suckers protruded very conspicuously and the body was much smaller in caliber 
than in the specimens from the salmon and the smelt. Yet in the absence of 
any structural differences I am forced to conclude that this contrast in size and 
general external appearance is due to some slight difference in the technique 
employed or in the condition of the parasites when they were preser\'ed. This 
is all the more probable when one considers that in one case the specimens from 
Esox were identical in appearance with those from the salmon. This parasite 
was found in all but one of the dozen specimens of Esox reiiculaius examined, 
being present in the stomach in numbers of i to 80 in each host. In two cases 
a single specimen was found in the intestine, perhaps due to some post-mortem 
wandering on the part of the parasites. In 4 specimens oi Anguilla cluysypa 
out of 9 examined I also found Azygia sebago in the stomach, but in small num- 
bers only, averaging 3 to each host. Finally 2 of these distomes were found 
in a single Pcrca flavescens, here also in the stomach. 

In order to give a ready comparison, I append hereto a table of similar 
measurements from a series of this distome taken from the various hosts men- 
tioned. The difference in length indicates in part age and in part method of 
preservation. In fact, it is difficult to achieve any uniformity among speci- 
mens so exceedingly active as this species. 

Measurements of Azygia sebago. 



Serial 

No. 


Host. 


Length. 


Ante- 
tip to 

cen- 
ter of 

oral 
sucker. 


Diam- 
eter 
of oral 
sucker. 


Dis- 
tance 

be- 
tween 

ters of 
suck- 


Diam- 
eter 
of ace- 
tabu- 
lum. 


Ante- 
tip to 

ter of 
ovary. 


Dis- 
tance 

be- 
tween 

ter"of 
ovary 
and 
ante- 

testis. 


Dis- 
tance 

be- 
tween 

ters of 
testes. 


Dis- 
tance 
from 
poste- 

testis 
to pos- 
terior 
tip. 


Breadth 
between 
suckers. 


Breadth 
behind 
acetab- 
ulum. 


Breadth 
behind 
poste- 

testis. 


16 
74-79 
60 
96 
7-8 
46 


From Salmo _ . . 

From Osmerus. 

do 

do." 

From Esox 

From Perca 


M,n. 
8.7S 
2.8s 
1.64 

4.08 


Aim. 

"""38" 
. 29 


Mm. 

0. 74 

■ 4 
.25 
.56 

■ 72 
• 51 

by. 57 


Mm. 
1.38 
.62 

■4 

"l"84' 
.78 


Mm. 

0.6s 
.33 

■ 37 

• 55 

.35 

by . 4 


Mm. 

4.76 
1.6 
.89 


Mm. 
0.31 


Mm. 

0. 62 


Mm. 

307 

■ 55 


Mm. 
I. 29 
.6s 

:Vs 

■ 75 
• 71 


Mm. Mm. 
1. 38 1.23 

:^8 -.W 


7.88 
2.69 


.9 

■ IS 


■ 91 
• 19 


3.25 
I. 16 


■ 77 
. 77 


• -4 
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a Much elongated: poor technique: preserved by helpe: 



The question naturally presents itself, Has this form been seen by others 
previous to the present date? The records on the subject are scanty, but they 
throw some light on the question. 



INTERNAL PARASITES OF THE SEBAGO SALMON. I183 

Leidy has described (1851, p. 206) a form as Disioinum ierreticolle '^ Rudolphi, 
which Pratt (1902, p. 957) lists as Azygia tereticollis (R.) Leidy. The original 
description is as follows (Leidy, 1851, p. 206) : 

Distomum terreticolle, Rud. Entoz. Syn., p. 102; Dujardin, Hist. Nat. des Helm.; 
Diesing, Syst. Helm., p. 358. 

Body subcylindric, light flesh color, posteriorly rounded. \'entral acetabulum (^ 
line) 1.6 mm. behind the oral (!^ line) 0.7 mm. in diameter. Oral acetabulum ('^ line) 
0.5 mm. 

Length (8 lines) 16.8 mm.; breadth posteriorly {% line) i mm., anteriorly ('^ line) 
0.7 mm. 

Habitation. — Stomach of Esox rcticulaius Lesueur. 

Remark. — The generative aperture is placed immediately in advance of the ventral 
acetabulum. When the animal contracts, the two acetabula are nearly brought into 
contact. 

The description is scanty, and yet one can say with some assurance that the 
form before Leidy was not the European species named by Rudolphi and dis- 
cussed by a long series of authors, of whom Looss (1894) has given the most 
complete description with truly admirable figures. Leidy's specimen is much 
too small for average adults of Azygia tereticollis, which is, moreover, cylindrical 
instead of broader posteriorly, as was Leidy's worm. Again, Azygia tereticollis 
has the oral sucker larger than the acetabulum, whereas in Leidy's form the 
reverse is true. Finally the suckers in Leidy's form do not agree at all in size 
with the suckers in Azygia tereticollis, as described by Dujardin and others. 

It is somewhat more diffictilt to say whether the form before Leidy was the 
same as that I collected in the Sebago salmon. In size the two are not very 
different, although Leidy's was larger. Other measurements do not agree at 
all well. The sizes given for the suckers are just about reversed. The final 
determination of this point, however, must await a reexamination of Leidy's 
original material. 

The only other reference to the occurrence of Azygia on this continent, so far 
as I know, is the brief note of Stafford (1904, p. 488) , in which he records Azygia ^ 
tereticollis Rudolphi from mouth, pharynx, oesophagus, and stomach of Esox 
lucius Linnaeus, Lota maculosa Le Sueur, and Ameiurus nigricans Le Sueur. 
Absolutely the onlv data concerning the worm which Stafford records is the size, 
12 by I mm. Now, this does not agree with adults of -4. tereticollis, for Looss 
(1894, p. 18) says of that species that the first eggs are not set free into the 
uterus until the worm is 8 to 10 mm. or more in length, and these are uniformly 
abnormal and defective. In another place he remarks (1894, p. 7) that in most 
cases eggs are found in worms 12 mm. long, although in scanty numbers. I 
am of the opinion that Stafford did not have before him the true .4. tereticollis 

a The text by error contains terreticolle for the specific name instead of tereticolle. 
6 Unfortunately, Stafford spells the genus Azigia and the species tereticolle. 



Il84 BULLETIX OF THE BUREAU OF FISHERIES. 

and incline to the belief that the form which he observed may have been the 
species under discussion. 

The European species, . I £:ji'(7/a tereticol lis, has been reported homEsoxlucius, 
Lucioperca sandra, Lota vulgaris, Truita variabilis, Saimo trutta, Salmo fario, 
Salmo hucho, Salmo alpinus, and Salmo salar. All of these save Salmo salar are 
fresh-water fish, and the parasite may be regarded as a characteristic of fresh- 
water species. The American species, Azygia sebago, I found in Salmo sebago, 
Esox reticulatus, Osmerus mordax, Anguilla chrysypa, and Perca flavescens. 
Stafford recorded what may have been the same from Esox lucius. Lota maculosa, 
and Ameiurus nigricans. These include strictly fresh-water forms, landlocked 
species, and one migratory fish, but inasmuch as the records have been taken in 
fresh water even the last host does not constitute any evidence against the fresh- 
water habitat of Azygia sebago. Its congener, Azygia tereticollis , found by 
Mcintosh in the salmon of the Tay, formed part of the evidence that this host 
feeds during its fresh-water residence. Equally here we may regard A. sebago 
as a fresh-water element acquired by its host since the latter became landlocked 
in Lake Sebago. The presence of the parasite in several other characteristic 
fish of the same water basin is clear evidence of the sources from which it might 
have come. 

CESTODES. 

Cestodes constituted the most conspicuous element of the parasitic fauna. 
Every salmon opened contained a mass of large worms in the pyloric region. 
They lay with the head and anterior portion of the body in a pyloric coecum 
usually at or near its tip. The worms were large and the body was thrown into 
loops which occupied the initial coecum and folded through the intestinal canal 
into other ca'ca, often crowding them full apparently to bursting. Viewed from 
the body cavity, even before the viscera were opened, one could distinguish the 
coeca which contained the parasites by their opaque, chalky appearance in distinct 
contrast with the translucent character of those coeca in which there were no 
tapeworms. When the intestine was opened it appeared full of the cestodes, 
which protruded in loops hanging from the coeca into the cavity or crossing into 
other coeca in a tangled mass, in several cases large enough to distend the wall 
conspicuously. The anterior coeca were those primarily or chiefly occupied by 
the worms and although often the entire cavity of the intestinal canal was 
crowded full of parasites, it was noteworthy that they rarely if ever entered any 
of the posterior coeca. When few worms were found they lay with the scolices 
at least in the coeca of the most anterior region. 

The species to which I have referred in the preceding paragraph is the well- 
known Bothriocephalus infundibuliformis, according to Liihe (1899) more cor- 
rectly designated Abothrium crassum, which is so common in the Atlantic salmon 



INTERNAL PARASITES OF THE SEBAGO SALMON. II 85 

from various parts of Europe. Of its occurrence in the Rhine salmon, where it 
is found in 42 per cent of the specimens examined, in 91 per cent of the Baltic 
salmon, in 26 per cent of the Tweed salmon, in most of the Tay salmon and of 
the Irish salmon, enough has been said in the historical survey. It is a typical 
salmonid parasite, and is found even in eight species of that family which inhabit 
fresh water. Its presence in the landlocked Salmo scbago, which confines its 
life cycle to fresh water, is hence not surprising. Evidently the life cycle of the 
species permits of easy adaptation to a fresh-water existence, for I have to report 
its occurrence not only in the host under discussion, but also in another promi- 
nent American salmonid, the Great Lakes trout, Cristivomcr namaycush (Wal- 
baum). It was found abundantly in specimens of this host which I examined 
in July and August, 1894, at Charlevoix, Mich. From 30 to 80 tapeworms of 
this species were present in each Sebago salmon, and neither size nor age played 
any evident part in determining the degree of infestation. Absolutely every 
one of the salmon taken was infested. In considering the possible life history, 
I naturally turned to the Sebago smelt as the host of the larval form, probably a 
plerocercoid, and examined a number of these fish with great care, but was 
unable to detect the lar^^a, if indeed it was present. Nothing was discovered 
which throws any light on the life cycle. It is worthy of note that all of these 
parasites were full grown; not a single specimen was found which was not dis- 
charging ripe proglottids. Consequently the infestation must have taken place 
somewhat earlier in the year. It would take observations at other months to 
determine when; and the food at that time would evidently be the source of 
the parasite. 

In addition to this dominant species some other cestodes were also recorded. 
A few fragments of a small species of Proteocephalus were found in each of four 
hosts, and a larval form, which probably belongs to the same Proteocephalus, 
was obtained in each of two hosts. Two different bothriocephalid larvae of 
small size also occurred each in a single salmon. The four forms just mentioned 
were all found in the intestine. 

The insignificant size of a new species of Proteocephalus found and the small 
number of individuals present in any one host resulted in its being overlooked 
at first, and it may easily have been present in more hosts than shown by the 
records. It was found in four out of the seven salmon examined, but in one 
case only a few loose proglottids were discovered by accident among material 
from the intestine. A careful examination in comparison with the descriptions 
of known species leads me to the view that this is a new species to which the 
name Proteocephalus pusillus may be given. The salient points in the descrip- 
tion of this new species are as follows: 

Proteocephalus pusillus nov. spec. — Adult cestode with short strobila, meas- 
uring only 30 to 50 mm. in length. Proglottids scanty, segmentation 



1 1 86 BULLETIN OF THE BUREAU OF FISHERIES, 

distinct. Head much contracted. Neck i to 1.5 mm. long by 0.21 mm. broad. 
First proglottids 0.09 mm. broad, changing gradually until in mature proglottids 
the length greatly exceeds the breadth. Ripe proglottids measure 0.84 to 1.4 
mm. long by 0.18 to 0.35 mm. broad. Terminal proglottids present and fertile. 
Sexual organs typical for Proteoceplialiis; uterus median, with 10 to 14 lateral 
outpocketings on either side. Testes numerous, within vitellaria. Genital pore 
lateral, one-third to two-fifths of length of proglottid from anterior margin of 
same. Ovaries bilobed, median isthmus indistinct, anteroposterior diameter 
nearly equal to breadth of both lobes. Only a few specimens obtained from a 
single host species, Salmo sebago. 

This species approaches most nearly to P. ocellata and P. percce among 
known species. Unlike the new species, however, both of these older forms have 
a fifth sucker, fewer lateral uterine outpocketings, a longer neck, differently 
shaped ovaries, and markedly different proglottids. 

In specimens wnth developed proglottids the head was so much contracted 
or distorted that any special description would be of little value. One could easily 
observe the general features characteristic of the genus. There was no well 
developed terminal or fifth sucker, and the end organ, which is known to replace 
it in many forms of this genus, was inconspicuously developed, if present. 
Personally, I incline to the view that on more careful examination this structure 
will be found in all species, even those in which its absence has been made a 
matter of record. Accordingly, not much weight can be put in its presence or 
absence in any individual case." 

Three plerocercoid larvae or young cestodes were found in company with 
Proteocephalus pusillus, which I regard as young forms of this species. The 
largest came from the salmon which was most heavily infected with this cestode 
parasite. It was 3.15 mm. long and had begun to assume clearly the appear- 
ance of an immature cestode. The head measured 0.3 mm. wide by 0.26 mm. 
long, and the suckers 0.14 mm. in length by o.ii mm. in width. The neck 
was slightly narrower than the head, but was not clearly set off from the body, 
which was very uniform in diameter and measured 0.25 mm. in average width. 
The posterior end of the body was swollen into a rounded knob about 0.35 mm. 
broad and of approximately the same length. This feature was evidently 
produced by a powerful contraction of the terminal region of the body. In 
and near it one could see very indistinct indications of proglottid formation. 
In form, size, and general aspect this young cestode was in full agreement with 
the anterior regions of the mature cestodes of this species with which it was 

oFor a more definite discussion of this peculiar structure so variable in development in the cestodes 
of this genus, I would refer to a paper now in press by my student, Mr. George R. La Rue, to whom 
I am indebted for a comparison of this material from Salmo sebago with preparations of other species 
of Proteocephalus 



INTERNAL PARASITES OF THE SEBAGO SALMON. II 87 

associated. The head, which was not contracted, showed on careful study the 
deUcate outhne of a rudimentary end organ. While such a structure was not 
demonstrated in the mature individuals described above, one can say positively 
that if present it could not have been seen owing to the greatly contracted 
condition of the adult scolices. I believe that its presence will be demonstrated 
in more favorable specimens. The complete agreement of this largest larva 
with the mature specimens in all other features compels me to regard both as 
different stages in the development of the same species. 

The other larvae were still in early stages of development, and probably 
had been ingested by the salmon at a very recent date. Their relationship is 
not so clear in all respects, and yet I do not hesitate to associate with the new 
species of Protcocephalus a plerocercoid or young cestode obtained from the 
same host as the adult worms and the older larva just described. The head is 
broadly conical, without furrows, and measures 0.3 mm. in breadth. The 
suckers measure 60 to 75/x in diameter. There is no rostellum or fifth sucker 
to be found, while the end organ is so poorly developed as to be visible with 
difficulty and only under the most favorable circumstances. The neck is 
nearly as broad as the head. In general appearance this larva resembles the 
adult cestode and the older larv^a previously described. With some reserve one 
may also assign to this species a single plerocercus taken from another specimen 
of Sahno sebago. The head, which measures only 1501J, in breadth, is shaped 
like that of the young cestode and like it is without rostellum or fifth sucker, 
while the end organ is difficult to demonstrate. Neither furrows nor ridges are 
seen on the larva, which has a total length of 1.14 mm. The sucker measures 
only 30 to 45/i in diameter. The neck is slightly narrower than the head. 
This form certainly belongs to the genus Protcocephalus and probablv to the 
species already described. 

From the scantiness of the material obtained one might infer that the 
Sebago salmon is only a casual host of the species. Yet I did not secure this 
parasite from any other fish in Lake Sebago and adjacent waters, and I have 
not met it in fish examined in other places. The presence of larvae in different 
stages of development with only a few adult specimens in any one host, 
although some were found in the majority of the salmon examined, would 
rather favor the view that the cestode was a regular though infrequent parasite 
of this host. 

Sparganum sebago, nov. spec. — In addition to the cestodes already men- 
tioned, there are to be noted two specimens of bothriocephalid larvae which 
deserve more extended mention. 

The first was taken from the spleen of one salmon. It measured 25 mm. 
in length and 1.8 mm. in maximum diameter. There is no neck, but the bodv 



1 1 88 BULLETIN OF THE BUREAU OF FISHERIES. 

increases slightly in breadth for about one-quarter of the entire length and 
then tapers gradually to the posterior end, which is rounded off. The body 
is elliptical in cross section without any segmentation, but with numerous rather 
prominent annular wrinkles. It seemed as if the margins of the body were 
thicker than the center. The head was retracted. (Fig. 7 and 8, pi. cxxi.) 

The second specimen (fig. 9 and 10, pi. cxxi) was found free in the body 
cavity of another salmon. It was 36 mm. long and 0.86 mm. in breadth. The 
body was somewhat thicker than in the other specimen, but less deeply wrinkled, 
and the center was certainly thicker than the margins. In this, as in the color 
and texture, it appeared different from the first specimen. There was no neck. 
The head measured 0.31 mm. in transverse diameter and 0.43 mm. from the 
apex to the base of the grooves, which were keyhole shaped. The groove 
measured 0.25 mm. in transverse diameter at the anterior end and 0.09 near 
its posterior end. In spite of the differences in appearance noted above it is 
easily possible that the two specimens belong to the same species and I have 
preferred to list them for the present under a single heading, naming the form 
Sparganum scbago. 

A word should be said with regard to other hosts for these cestodes. 
Abothrium crassum was not found in any other fish examined at Sebago Lake. 
Larvae of Proteocephalus and of some bothriocephalid were found in a very few 
cases in other fish taken from these waters. There were none, however, of 
which it could be said with reasonable certainty that they were the same as the 
forms collected from the vSebago salmon and mentioned above. The question 
of the occurrence of such salmon parasites in other hosts of this region must be 
left entirely open for the present at least. 

NEMATODES. 

Nematodes were not common. They occurred only in half of the specimens 
of salmon examined and were not abundant. In one salmon t,^ of these worms 
were obtained, but in the other three only a dozen all told. Accordingly they 
seem to play only a minor part in the parasitic fauna of the Sebago salmon. 
They belong to two or three separate species, which are radically distinct. Thus 
far I have not been able to make a satisfactory determination for any of them, 
owing to the scantiness of the material and to its unsatisfactory condition. 
This much can be said: They do not belong to any of the species, or even to 
the genera, heretofore recorded for the Atlantic salmon. A few notes may be 
added here concerning these forms. 

A small nematode was found in the stomach and in the body cavity of two 
salmon. In all there were only six individuals of this species. I have not been 
able to satisfy myself that the individuals recorded as from the stomach 
really belong there, but incline to think that they were adherent to the external 



INTERNAL PARASITES OF THE SEBAGO SALMON. I189 

surface of the stomach and passed unnoticed when that organ was opened and 
shaken in a preserving fluid in order to collect the small specimens of Azygia 
sebago concealed in the gastric mucus. Subsequently they were found in the 
material obtained in this process. They are probably true parasites of the 
body cavity. Since an approximate determination may easily be misleading I 
forego all attempt to name this form and designate it for the present simply 
as "Nematode A." 

The group of t,t, nematodes obtained from the body cavity was a source of 
great surprise. These worms are identical with a form found in very large num- 
bers in the Alaska salmon. Since, however, this species is to be discussed at 
length in the section of my report which deals with that host, it seems wise to omit 
here any details and refer to the worm simply as "Nematode B." It is a large 
form belonging to the Filariadae, but so delicate that it is almost impossible to 
obtain perfect specimens, and it has thus far proved beyond my skill to preserve 
any in a complete condition. It has been an exceedingly interesting object of 
study and will receive at an early date, in connection with the records of the 
Alaska salmon and its parasites, that detailed consideration which its frequence 
and its interest warrant. The six nematodes recorded from the stomach were 
collected and preserv^ed by an assistant. They are in very poor condition, 
so that any determination can hardly be more than an impression, but the 
only real reason why I hesitate to refer them to the same species is that in all the 
thousands of specimens from nearly 200 hosts which I handled in the course of 
my investigations on the Alaska salmon I never once found the species any- 
where save in the body cavity. It is not impossible that these specimens were 
reported from the stomach through some error. As repeated examination is 
bringing me more and more firmly to accept the identity of this lot with those 
which I collected personally from the body cavity of the Sebago salmon and 
of the Alaska salmon, I am being forced to assume the existence of some error 
in recording them as from the stomach. 

In any event, it may be said that not more than three species of nematodes 
are present in the Sebago salmon and that these species are only infrequently 
and scantily represented in this host. None of the nematodes were found in 
any other fish examined at Sebago Lake, nor are they known to me from fish 
of any fresh-water locality in this country. Thus far also I have failed to find 
any reference in the literature which could be construed as indicating either 
of these forms. 

RESUME AND CONCLUSIONS. 

The first general conclusion to be drawn from this study of the parasitic 
fauna of the Sebago salmon is that the total number of parasites recorded 
from this host is small. In all, there have been listed only i trematode, 2 
cestodes, 4 (?) cestode larvae, and 2 nematodes, or a total at most of 9 species 



1 1 go BULI^ETIN OF THE BUREAU OF FISHERIES. 

of parasites. To be sure, the number of hosts examined was small, and 
this mav account for the low total record. Two of these parasites, Azygia 
sebago and Abothriiim crassum, were found in every fish examined, and each of 
six other parasites was found in two hosts. This may be compared with 
Zschokke (1S96, p. 824), who records the parasitic census of losalmon from the 
North Sea. In these 10 fish were found 10 species of parasites. A trematode 
and a cestode occurred each in 9 of the fish examined. The cestode was 
Abothrium crassum, the same species as that found in every Sebago salmon; 
the trematode was Distomum ocreaiuni, a purely marine form, and hence in 
sharp contrast with the abundant trematode in the Sebago salmon, which is 
a member of a characteristic fresh-water genus. This contrast, as well as 
several other details commented on in the previous pages, seem to indicate 
the fresh-water aspect of the parasitic fauna in the Sebago salmon. 

The conditions in the Sebago salmon are all the more striking when one 
considers the forms which are not found among its parasites. Reverting first 
to the trematodes, one notices that the only genus represented luere, Azygia, 
has been recorded from the Atlantic salmon in Europe only in a single case, 
while here its representatives were found in every host examined. On the other 
hand, Derogenes varicus, recorded from a good percentage of European salmon 
in all localities, was not seen even once. The other distomes recorded by 
European observers in various regions, and often as fairly frequent parasites 
of the salmon, are entirely wanting in Sebago salmon. Azygia is the only 
purely fresh- water distome found in European salmon; it is the only distome 
found in the Sebago salmon. The other distomes recorded in European salmon 
are purely marine species, or very largely so, but none of them occur in the 
Sebago salmon. 

Among the cestodes conditions are identical. The common form, Abothrium 
crassum, is confined to salmonids, without reference to their habitat, and is as 
common in fresh-water species as in marine. On the other hand, those cestodes 
which are typically marine, like Rhynchobotlirium paleaceum, Scolex polymorphus, 
and the several species of Tctrarhynchus, are absolutely wanting in the vSebago 
salmon. The various cestode lars^ae are too little known to justify their con- 
sideration in this connection. They are not referable, even indefinitely, to 
either habitat. To this statement one must make two exceptions. Scolex 
polymorphus, recorded from the salmon in Europe, is typically marine, occurring 
in many sea fish, even though several species may be indicated under the single 
name. On the other hand, the larva of Proieocephalus is equally typically 
limnetic and it is recorded from the Sebago salmon only unless the single record 
of Tania sp. for a larva from the salmon in the Tweed should be referred to 
this form. In this group again it appears clear that the marine parasites of the 
European salmon are wanting in the Sebago species, that the only cestodes 



INTERNAL PARASITES OF THE SEBAGO SALMON. II9I 

identical in the two forms are such as are clearly fresh-water species, and that 
the Sebago salmon contain at least one clearly fresh-water genus which is not 
reported from the corresponding European host. 

Among the nematodes the evidence is less conclusive, since the amount of 
material is smaller; .indeed, hardly enough to form a basis for any conclusions. 
At the same time, all the species which give to the parasitic fauna of the European 
salmon its marine aspect are entirely wanting here. Not a single specimen of 
Agamonema was discovered, although two species are found in the European 
salmon, and one of them, Agamonema capsularia, is very common. Both Ascaris 
and Echinorhynchus are unrepresented in the parasitic fauna of the Sebago 
salmon. Among the numerous species of each already recorded as parasitic in 
the European salmon three out of four are purely marine. Here again one 
notes that the marine elements in the parasitic fauna of the European salmon 
are wanting in the Sebago salmon. Possibly the large filariad found abun- 
dantly in the Alaska salmon, and reported also from one or two salmon taken in 
Sebago Lake, forms an exception to the general rule. As I have already noted, 
it appears to be marine in origin. This may be, however, a false argument, 
and the species may actually be one limited to this host or to the salmonid 
family, regardless of habitat. In this connection one naturally recalls at once 
the case of Abothrium crassjiin, which, from the observations on salmon in the 
North Sea and then in the Rhine, might be said to be a marine form, since it 
gradually disappears on the journey up the Rhine. But it occurs in hosts of 
purely fresh-water habitat, such as Salmo hucho in Europe and Cristivomer 
namaycush in the Great Lakes of North America. Evidently further informa- 
tion is needed before one can safely assign this nematode to a definite habitat. 

Summing up all the evidence concerning the parasites of the Sebago salmon, 
one finds that four species are unknown in character, one only is possibly marine, 
•one is a pure salmon parasite, and three are clearly fresh-water forms. The 
latter are also its most frequent and numerous guests. Furthermore, the 
Sebago salmon lacks every one of those parasites found in the European salmon 
which must be regarded as purely or largely marine, and possesses in common 
with its European congener only one characteristic salmon parasite and possibly 
also two fresh-water forms, which, though abundant in its own parasitic fauna, 
are very rare in that of its relative. 

The parasitic fauna of the Sebago salmon manifests a striking fresh-water 
aspect, all the more unexpected in view of the marine character of that in the 
European salmon as demonstrated by Zschokke. One could hardly find a more 
convincing demonstration of the fundamental biological relation between parasite 
and host. 

The parasitic fauna of any animal is primarily a function of its habitat. 



1 192 BULLETIN OF THE BUREAU OF FISHERIES. 

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1893. Life history of the salmon. Bulletin LI. S. Fish Commission, vol. xiii, p. 21-38. 

Bellingham, O. 

1840. Catalogue of the Entozoa indigenous to Ireland. Magazine of Natural History, n. s., vol. 

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1844. Catalogue of the Entozoa indigenous to Ireland. (Reprinted.) Annals and Magazine of 

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GoEZE, J. A. E. 

1782. Yersuch einer Naturgeschichte der Eingeweidewiirmer thierischer Korper. 471 p., 35 pi. 
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1899. Neuere Lachs- und Maifisch-Studien. Tijdschrift der Nederlandsche Dierkundige Vereeni- 
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Jordan, D. S., and Evermann, B. W. 

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4 
Leidv, J. 

1 85 1. Contributions to helminthology. Proceedings Academy of Natural Science, Philadelphia, 

vol. 5, p. 205-210. 
1871. Notices of some worms, Dibothrium cordicefa, Hirudo, Gordius. Ibid., vol. it,, p. 305-307. 

LiNSTOW, O. von 

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bd. 12, p. 521-784, 9 taf. 
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Jahrbiicher, Systematik, bd. 26, p. 63-180, 9 taf. 



INTERNAL PARASITES OF THE SEBAGO SALMON. II 93 

LtJHE, M. 

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1 1 94 BULLETIN OF THE BUREAU OF FISHERIES. 

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1896. Zur Faunistik der parasitischen Wiirmer von Siisswasserfischen. Ibid., bd. 19, p. 772-784, 
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EXPLANATION OF PLATE. 

Fig. I. Azygia sehago. Group of individuals from Salmo sehago, after preservation in corrosive sub- 
limate and then alcohol. X2. 

2. Azygia sehago. Specimen from salmon, stained and mounted in balsam. Dorsal view. Xi2>^. 

3. Azygia sehago. Anterior region of alimentary canal in lateral aspect. Reconstruction by 

Messrs. W. M. Anderson and H. B Boyden. in, intestine; ce, oesophagus; as, oral sucker; 
ph, pharynx. Highly magnified. 

4. Azygia sehago. Longiscction showing relations of principal organs, exc, main excretory 

vessels; Ipm, longitudinal parenchym muscles, for explanation of which compare text; vit, 
follicles of vitellarium. Camera drawing. X358. 

5. Azygia sehago. Female reproductive system in dorsal aspect. Semidiagrammatic to show 

relation of organs in ovarial complex. Ic, Laurer's canal; od, germ duct; ov, germarium; 
sg, shell gland; iit, first coils of uterus; yd, transverse vitelline duct; yr, yolk reservoir. 
After reconstruction by Messrs. Anderson and Boyden. Highly magnified. 

6. Azygia sehago. Transsection through ovarial complex, showing relations of organs to common 

capsule (see text), in, intestinal crura; Ipm, longitudinal parenchym muscles; ov, germ 
gland; sg, shell gland; ut, first coil of uterus; vii, follicle of vitellarium; yd, common yolk duct 
and part of yolk reservoir. Camera drawing X60. 

7. Sparganum sehago, nov. sp. Bothriocephalid larva from spleen of Salmo sehago. Drawn from 

alcoholic specimen. X2. 

8. Head of larva, shown in fig. 7 X25. 

9. Sparganum sehago, nov. sp. Bothriocephalid larva from body cavity of Salmo sehago. Drawn 

from alcoholic specimen. X2. 
10. Head of larva, shown in fig. 9. X25. 



BuL. U. S. V,. F., 190.S. 



Pl.ATK CXXI. 




